Penalba Et Al 2024 Hybridizationreview

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The Role of Hybridization in Species Formation

and Persistence
Joshua V. Peñalba,1 Anna Runemark,2 Joana I. Meier,3,4 Pooja Singh,5,6

Guinevere O.U. Wogan,7 Rosa Sánchez-Guillén,8 James Mallet,9 Sina J. Rometsch,10,11
Mitra Menon,12 Ole Seehausen,5,6 Jonna Kulmuni,13,14,16 and Ricardo J. Pereira15,16
1
Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Center for Integrative
Biodiversity Discovery, 10115 Berlin, Germany
2
Department of Biology, Lund University, 22632 Lund, Sweden
3
Tree of Life, Wellcome Sanger Institute, Hinxton, Cambridgeshire CB10 1SA, United Kingdom
4
Department of Zoology, University of Cambridge, Cambridgeshire CB2 3EJ, United Kingdom
5
Department of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, 3012 Bern,
Switzerland
6
Center for Ecology, Evolution & Biogeochemistry, Swiss Federal Institute of Aquatic Science and Technology
(EAWAG), CH-8600 Kastanienbaum, Switzerland
7
Department of Integrative Biology, Oklahoma State University, Stillwater, Oklahoma 74078, USA
8
Red de Biología Evolutiva, INECOL, Xalapa, Veracruz, CP 91073, Mexico
9
Organismal and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA
10
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06511, USA
11
Yale Institute for Biospheric Studies, Yale University, New Haven, Connecticut 06511, USA
12
Department of Evolution and Ecology, University of California Davis, Davis, California 95616, USA
13
Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics,
University of Amsterdam, 1098 XH Amsterdam, The Netherlands
14
Organismal and Evolutionary Biology Research Programme, University of Helsinki, Biocenter 3, Helsinki,
Finland
15
Department of Zoology, State Museum of Natural History Stuttgart, Stuttgart 70191, Germany
Correspondence: ricardojn.pereira@gmail.com
Hybridization, or interbreeding between different taxa, was traditionally considered to be rare

and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown
of reproductive isolation and even to the reversal of speciation. However, modern genomic
and analytical methods have shown that hybridization is common in some of the most diverse
clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to
introgression of adaptive alleles, to the formation of hybrid species, and even to entire species
radiations. In this review, we identify consensus among diverse research programs to show
how the field has progressed. Hybridization is a multifaceted evolutionary process that can
strongly influence species formation and facilitate adaptation and persistence of species in a
rapidly changing world. Progress on testing this hypothesis will require cooperation among
different subdisciplines.
16
These authors contributed equally to this work.
Editors: Catherine L. Peichel, Daniel I. Bolnick, Åke Brännström, Ulf Dieckmann, and Rebecca J. Safran
Additional Perspectives on Speciation available at www.cshperspectives.org
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J.V. Peñalba et al.
T he origin of species and the role that “hybrid-

ization” plays in it has been of significant
interest in evolutionary biology throughout
sophila species. Numerous comparative stud-
ies in insects (Sánchez-Guillén et al. 2014),
amphibians (Sasa et al. 1998; Pereira and Wake
the years. Hybridization is now recognized to 2009), fishes (Bolnick and Near 2005; Stelkens
be widespread in nature (Whitney et al. 2010; et al. 2010), birds (Price and Bouvier 2002),
Shurtliff 2013; Taylor and Larson 2019; mammals (Adavoudi and Pilot 2021), and an-
McEntee et al. 2020) and modern genomic giosperms (Moyle et al. 2004) show similar pat-
methods have revealed that ancient hybridiza- terns. However, the strength of this correlation
tion (Box 1),17 and subsequent “introgression” is complicated by effects of sex determination
or “gene flow,” has been prevalent during the (Stöck et al. 2021), sexual selection (Rosenthal
evolution of many taxa (Sankararaman et al. 2013), sexual conflict (Martin and Hosken 2003),
2014; Irisarri et al. 2018; Suvorov et al. 2022). and mating system (selfing vs. outcrossing spe-
Because “reproductive isolation” typically takes cies; Pickup et al. 2019), among other factors.
a long time to build up (Coyne and Orr 2004; For example, plants have been suggested to hy-
Dopman et al. 2023) relative to the rate of bridize at greater levels of genetic divergence
geographic range change, there are opportuni- than animals possibly because they are able to
ties for species to hybridize throughout much self-fertilize and become allopolyploids (Chap-
of their evolutionary history (Fig. 1A). Such man and Burke 2007). Meta-analyses including
hybridization can have important evolutionary systems with different mating and sex-determi-
consequences, for example, facilitating reinforce- nation systems are needed to elucidate how these
ment selection for assortative mating (Dobzhan- factors impact the relationship between diver-
sky 1937b; Yukilevich et al. 2023), weakening gence and probability of hybridization.
or removing these barriers to gene flow (Behm “Hybrid zones” are narrow regions in which
et al. 2010; Kearns et al. 2018), producing novel individuals of genetically distinct groups meet,
phenotypes (Rieseberg et al. 1999a), permitting mate, and produce offspring of mixed ancestry
the evolution of new independent evolutionary (Harrison 1990). Hybridization often occurs in
lineages (Olave et al. 2022), or facilitating adap- areas of inferred secondary contact, especially at
tive radiations (Seehausen 2004). the edges of biogeographical regions (e.g., coral
The term hybridization is often reserved for reef fishes [Hobbs and Allen 2014]) or at bio-
mating between species. However, the boundary geographic barriers (e.g., Amazon River [Rosser
between diverging populations and species is et al. 2021]). Geographic areas where many spe-
often unclear, such that it is more useful to dis- cies form hybrid zones, so-called suture zones
cuss hybridization as gene flow between genet- (Remington 1968; Hewitt 1988), have been at-
ically distinct lineages (Barton and Hewitt tributed to contact between lineages expanding
1985). We introduce the topic to readers new out of Pleistocene refugia in Europe (Hewitt
to the field by identifying recent advances that 2001), North America (Anderson 1953), and
are consistent across organisms and outline Australia (Moritz et al. 2009). These geographic
open questions that deserve future attention. areas provide an invaluable glimpse into the
speciation process, as pairs of taxa that differ
THE PROBABILITY OF HYBRIDIZATION in life history traits (e.g., dispersal rate, gen-
eration time) interact in the same extrinsic en-
The probability of hybridization can be predict- vironment (e.g., age and location of the suture
ed based on divergence to some extent (Roux zone).
et al. 2016). Coyne and Orr (1989) found a pos- Human-altered areas are also potentially
itive correlation between genetic divergence and more prone to hybridization. Habitat perturba-
strength of reproductive isolation among Dro- tion increases the chance of hybridization (e.g.,
due to lack of mate choice opportunities if pop-
17
Descriptions of text in quotes are listed in the Glossary ulation densities are low [Rohde et al. 2015]),
(Box 1). removal of physical or ecological barriers, or
2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a041445
Role of Hybridization in Species Formation
BOX 1. GLOSSARY
• Admixed—when contributions to the genome are from multiple genetically distinct ancestral
populations.
• Allopolyploid hybrid speciation—speciation by hybridization, where the new lineage has doubled
the chromosome number by combining chromosomes from the two parental species.
• Epistasis—functionally interacting alleles, such that their combined fitness deviates from linearity or
additivity.
• Gene flow—transfer of genes between populations (Slatkin 1985) following individual migration
between populations at any level of divergence. Gene flow between different taxa ( populations,
subspecies, or species) is synonymous with introgression.
• Genetic architecture—the underlying genetic basis of a particular trait referring to the number,
genomic locations, effect size, and interaction of genetic variants that contribute to the phenotype.
• Homoploid hybrid speciation, combinatorial speciation—hybrid speciation without increase in
ploidy.
• Hybrid species—lineage that arose due to hybridization between two (or more) species and that is
reproductively isolated from parental species (Grant 1981).
• Hybrid vigor and heterosis—when hybrids (or more heterozygous genotypes) are fitter than their
parents (or more homozygous genotypes).
• Hybrid zone—narrow geographic regions in which genetically differentiated populations with
parapatric distribution meet, mate, and produce at least some offspring of mixed ancestry
(Harrison 1990).
• Hybridization—reproduction between genetically distinct populations producing offspring of
mixed ancestry (Barton and Hewitt 1985).
• Introgression—incorporation of alleles from one population from another distinct, population via
hybridization (Anderson 1953).
• Linkage disequilibrium—nonrandom association of alleles from two or more loci on haplotypes
(Haldane 1919; Lewontin and Kojima 1960).
• Reproductive barriers—behavioral, ecological, temporal, mechanical, or intrinsic (e.g., inviability
or sterility of hybrids) barrier that reduces or prevents gene flow between taxa. Some researchers use
the term incompatibility to refer to all these barriers (as referred to in this article), while other authors
use incompatibility to exclusively refer to intrinsic incompatibilities resulting from gene–gene
coevolution.
• Reproductive isolation (RI)—reduction in potential gene flow between populations caused by
barriers to gene flow (Stankowski and Ravinet 2021). The term is used and measured in different
ways by different researchers (Westram et al. 2022).
• Speciation continuum—definitions differ among researchers (Stankowski and Ravinet 2021), but in
general the speciation continuum is a concept that acknowledges that speciation is a continuous
process, not a single, sudden event.
• Transgressive segregation—quantitative traits in segregating hybrid populations where phenotypes
are extreme relative to those of both parental lines (Rieseberg et al. 1999a).
loss of ecological niches (Vonlanthen et al. many new opportunities for hybridization. In
2012). Human-assisted movement of species some cases, hybridization between introduced
(e.g., for trade or cultivation) also provides and native species leads to invasive hybrid line-
Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a041445 3
A Species formation in time B Species as metapopulations
Time
C Phenotypic change over time D Phenotypic change over space
G. fortis G. scandens
1990 2003
1978
Figure 1. Hybridization over space and time. (A) Populations (light blue) and arbitrary species (dark blue)
splitting and merging through time with gene flow (black arrows). (B) Different shades of blue represent
genetically distinct populations with differing degrees of connectivity and gene flow across space. (C) An
empirical example where rate of hybridization and survival of hybrids varies across Geospiza fortis and Geospiza
scandens system (Grant and Grant 2008). The sun and clouds represent periods of drought and rainfall. The
arrow depicts gene flow during the period of rainfall. (D) An empirical example of phenotypic change and degree
of reproductive isolation among parapatric populations of the salamander Ensatina eschscholtzii ring species in
California (Pereira and Wake 2009). The “X” between the southern populations represents rare or no hybrid-
ization.
ages (Abbott and Lowe 2004; Ainouche et al. common if new niches exist that are unoccupi-
2004; Fitzpatrick et al. 2010), providing exciting ed by either parental species (Moore 1977;
systems to understand the genetic basis of adap- Rieseberg et al. 2003; Meier et al. 2017a; Di-
tation and invasiveness. Vittorio et al. 2020). Allopolyploid hybrids or
The probability of hybridization and persis- “hybrid species” are hypothesized to be com-
tence of hybrids can also be affected by the mon in extreme habitats such as the arctic
ecological context. For instance, “homoploid (Brochmann et al. 2004), perhaps due to shield-
hybrid speciation,” stable hybrid populations, ing against loss of genetic diversity in small, iso-
and radiation of hybrid lineages are all more lated populations.
The demographic context also affects the Underlying reproductive barriers are geno-
direction and degree of gene flow. If one mic regions referred to as barrier loci, hybrid
species is expanding its range into that of anoth- incompatibility loci, or sometimes speciation
er species, the invading species is likely to genes. These loci hinder introgression at and
become more “admixed.” This is because, at around their genomic location. The common
the expansion front, the invading species is view of hybrid incompatibilities are as negative
less common leading to asymmetric backcross- “epistatic” interactions between two or more
ing and gene flow toward the invasive species loci. The classic Bateson–Dobzhansky–Muller
(Excoffier et al. 2009). Moreover, range expan- incompatibility (BDMI) model postulates that
sions are predicted to lead to the accumulation derived alleles in one or more loci in one geno-
of slightly deleterious mutations at the expan- mic background are incompatible with derived
sion front, and consequently to the purging of alleles from another genomic background, re-
deleterious mutations following introgression ducing the fitness of hybrids between them
of more beneficial variants (MacPherson et (Bateson 1909; Dobzhansky 1936; Muller 1942;
al. 2022), a hypothesis that needs empirical Reifová et al. 2023). Although these authors ini-
testing. tially described BDMIs as potentially being
dependent or independent from the extrinsic
environment, BDMIs have been more common-
SPECIATION AND HYBRIDIZATION
ly treated as environment-independent (i.e., in-
During speciation, a reduction of free recombi- trinsic incompatibilities). Examples include hy-
nation and gene flow increases “linkage disequi- brid necrosis in plants (Bomblies and Weigel
librium” (i.e., coinheritance) within the genome 2007), mitonuclear incompatibilities in mice
and between the traits defining taxa (Butlin (Ma et al. 2016), or hybrid male sterility in fruit
2005; Servedio 2009). Hybridization, on the oth- flies (Masly and Presgraves 2007). In contrast,
er hand, combines divergent genomes and can the term “ecological incompatibility” is reserved
either break up coadapted allele combinations for coadapted alleles affecting traits that vary in
(Barton 2001) or lead to novel adaptive allele fitness in recombinants in an extrinsic ecologi-
combinations (Abbott et al. 2013; Marques cal context (see Thompson et al. 2023)—as in
et al. 2019; Runemark et al. 2019). Combina- stickleback fishes (Arnegard et al. 2014). Assor-
tions containing both beneficial and deleterious tative mating incompatibility describes incom-
alleles are created simultaneously upon hybrid- patibility between the gene(s) underlying a given
ization, and the interplay between these will de- phenotypic mating trait and the gene(s) under-
termine the overall fitness of hybrid genotypes lying the preference for that trait (see Merrill
(Kulmuni and Pamilo 2014; Pereira et al. 2014). et al. 2023). These can evolve via the Fisherian
Traits that cause low fitness in hybrids can con- runaway process of sexual selection, such as in
tribute to maintenance of genetic distinctiveness morphologically and ecologically similar species
of taxa by reducing gene flow between them. of Laupala crickets (Xu and Shaw 2019), or via
These are variously termed “reproductive barri- environment-dependent sensory drive selec-
ers” or hybrid incompatibilities, and can be be- tion, such as in ecologically divergent species
havioral, ecological, temporal, mechanical, or of cichlid fishes (Seehausen et al. 2008b). In-
genetic. The initial evolution of these traits is compatibilities resulting from these different se-
likely a by-product of divergence between pa- lective regimes may also differ in how they are
rental taxa. However, some barriers may also expected to decrease fitness in consecutive gen-
accumulate via “reinforcement of mating isola- erations of hybrids (Lindtke and Buerkle 2015).
tion” (Dobzhansky 1937a) if strong selection Multiple types of incompatibilities may be pre-
favors a reduction in gene flow. The mecha- sent, interacting, and evolving further in any
nisms by which barriers to gene flow arise and given pair of taxa (Kulmuni and Westram
the order at which they accumulate are under 2017). Additionally, the “genetic architecture”
intense research. (i.e., number, location, and overall fitness ef-
fects) of these incompatibilities will determine INSIGHTS ABOUT SPECIES BOUNDARIES

the overall degree of reproductive isolation
Most evolutionary biologists, whether adopting
(Bank et al. 2012; Ferris et al. 2017; Dagilis
phylogenetic, biological, recognition, or geno-
et al. 2019). More theoretical and empirical stud-
typic cluster concepts of species, agree that spe-
ies are needed to understand how incompatibil-
cies boundaries in sexual taxa are maintained by
ities arise, affect the evolution of other incom-
some combination of barriers to gene exchange.
patibilities, and ultimately restrict gene flow.
Hybridization can reveal the genes and genetic
Both speciation and hybridization occur in a
architecture of traits that are relevant to species
variety of temporal and geographic contexts
boundaries. As populations become increas-
(Fig. 1). What we observe today may mask a
ingly reproductively isolated, hybridization can
history of populations merging and splitting in
reveal how genomes differentiate and gene flow
the past (Mallet et al. 2016; Abbott 2019; He
becomes restricted. Hybridization provides
et al. 2019; Peñalba et al. 2019). Divergent line-
unique insight as it is often difficult to make
ages can be lost due to extinction or absorption
inferences about barriers to reproduction when
into another population (Zhang et al. 2019; Frei
populations are diverging in isolation.
et al. 2022), and changes in selection, the envi-
ronment or mating dynamics may affect these
Hybrids as Windows into the Genetic
outcomes (Feder et al. 2003; Han et al. 2017;
Basis of Species Boundaries
Nelson and Cresko 2018). Simplifying specia-
tion into bifurcating lineages may lead to inac- When hybridization occurs, rates of introgres-
curate reconstructions of evolutionary history, sion are expected to be heterogeneous along the
while estimates of historical gene flow may be genome, which allows one to identify genomic
spurious if the possibility of introgression from regions associated with species boundaries. Tra-
“ghost lineages” is ignored (Mallet et al. 2016; ditionally, most studies have used experimental
Barlow et al. 2018; Ottenburghs 2020; Tricou hybrids to reveal the phenotypic or fitness effect
et al. 2022). Researchers are expanding their fo- of an introgressed genomic region in a foreign
cus beyond the classical geographic modes of genomic background (Schumer et al. 2014a).
speciation (allopatry, parapatry, and sympatry) However, this approach is limited to taxa ame-
to incorporating demographic modes of speci- nable to laboratory culture, where organisms
ation that allow quantifying periods of diver- can be crossed over tens (e.g., flies [Masly and
gence with gene flow (Csilléry et al. 2010; Brad- Presgraves 2007]) or hundreds of generations
burd et al. 2016; Excoffier et al. 2021). We also (e.g., yeast [Burke et al. 2014]). An alternative
often study hybridization between a pair of pop- approach is to study taxa that hybridize in nature
ulations as representatives of the entire species. over a larger number of generations, increas-
The reality may often be more complex, involving recombinant variation among incompatibil-
ing a network of multiple populations across ity loci and linked neutral genomic regions (Tur-
the geography, some of which may hybridize ner and Harr 2014). Natural hybrids have the
with another taxon, whereas others do not advantage of being subject to selection and re-
(Fig. 1B). The variation in divergence and gene combination in an ecologically relevant setting,
flow among the subpopulations within the where multiple selective forces act simultane-
metapopulation as well as the influence of a giv- ously and interact (e.g., sexual selection, adapta-
en allele on fitness in different ecological con- tion, and gene coevolution). While incompati-
texts, may play an important role in determining bilities are expected to persist in hybrid zones,
the evolutionary trajectory of any given lineage. due to a balance between dispersal of parental
Further development in analytical approaches gene combinations and selection against hybrid
is needed to be able to simulate more com- combinations, these incompatibilities can quick-
plex two-dimensional configurations contain- ly be purged from hybrid populations that are
ing multiple populations (Bradburd and Ralph geographically isolated from their parentals (Li
2019; Harvey et al. 2019). et al. 2022), providing valuable systems to un-
derstand the genetic basis of hybrid breakdown late or break down, leading to a continuum of
and its recovery. reproductive isolation (Fig. 2; Stankowski and
Hybridizing species provide important in- Ravinet 2021). Many population pair compari-
sights into the nature of selection acting on spe- sons with varying degrees of reproductive isola-
cies boundaries that reduce gene flow between tion are needed to study a “speciation continu-
diverging taxa. For example, in sympatric birds um” and understand how a single population
(Toews et al. 2016; Turbek et al. 2021), butter- can diversify into multiple species over time.
flies (Merrill et al. 2019), and crickets (Xu and The correlation between genetic divergence
Shaw 2020), hybridizing taxa are maintained by and the ability to exchange genes (as a proxy
divergent male signaling and female preferences for reproductive isolation) across 61 taxa pairs
between species, suggesting that sexual selection at different stages of divergence suggests a gray
may have been involved in species formation zone of speciation where the likelihood of gene
(Svensson et al. 2017). Parapatric fish (Haenel flow is rapidly reduced (Roux et al. 2016). The
et al. 2021), monkeyflowers (Stankowski et al. sigmoidal transition between unrestricted gene
2019), and sunflowers (Todesco et al. 2020) flow and its abolition is consistent with the idea
show that species or ecotypes can also be main- of a tipping point (Nosil et al. 2017; Riesch et al.
tained by divergent selection coincident with 2017; Peñalba et al. 2019). The nonlinear time
environmental gradients, suggesting a role of course has been referred to as a snowball
ecological selection in species formation. Hy- of hybrid incompatibility (Orr 1995; Matute
bridizing mice (Turner and Harr 2014), weeds et al. 2010; Moyle and Nakazato 2010; see also
(Hämälä et al. 2017), and monkeyflowers (Fish- literature on coupling by Aubier et al. 2023;
man and Willis 2006) show low hybrid fitness in Dopman et al. 2023; Ritchie and Butlin 2023).
the form of sterility or reduced cognition, sug- This pattern also suggests that species that
gesting incompatible gene interactions are also have not accumulated sufficient barriers to
important in species formation (Coughlan and gene flow may be ephemeral and fuse back in-
Matute 2020). While strictly intrinsic incompat- to single lineages (Rosenblum et al. 2012; Frei
ibilities can only manifest as postmating barri- et al. 2022). However, the dynamics of incom-
ers, behavioral and ecological incompatibilities patibilities is challenging to study across taxa
can act as both premating barriers (McKinnon and there is ongoing debate about the generality
et al. 2004), and as postmating barriers that re- of tipping points in speciation (Barton and de
duce the reproductive fitness of hybrids (Gotts- Cara 2009). The theoretical expectation of non-
berger and Mayer 2007; Arnegard et al. 2014; linear patterns of barrier accumulation do not
Bay et al. 2017). The observation that alleles hold, for example, when species emerge from
underlying behavioral (Seehausen et al. 2008b; hybrid populations and incompatible gene in-
Meier et al. 2017a), ecological (Lamichhaney teractions emerge from sorting of standing var-
et al. 2015; Martinez Barrio et al. 2016), and iation (see sections below; Marques et al. 2019).
environment-independent intrinsic (Sicard et Wu (2001) suggested that speciation can be
al. 2015; Fuller et al. 2018) incompatibilities illustrated as a series of stages of divergence,
can be older than the split between sister taxa depicting how genome-wide differentiation
suggest that all these types of incompatibilities and linkage disequilibrium may build up (Fig.
may be present before the onset of speciation 2). In this simplified hypothesis, gene flow is
and may be segregating already in the ancestral unrestricted in a panmictic ancestral popula-
population. (Xie et al. 2007; Roberts Kingman tion, is increasingly restricted as more genes
et al. 2021). are involved in reproductive barriers, and be-
comes zero when reproductive isolation is com-
plete (see stages in Fig. 2F). Empirical studies
Hybridization and the Speciation Continuum
have now clarified that the transition between
Traits and loci reducing gene flow between di- these stages of divergence might be very fast
verging taxa are expected to gradually accumu- for sympatric radiations and that stages can
Population 1 Species 1 Demic perspective

A
Population 2 Species 2
B Speciation continuum
C Speciation reversal,
Probability of Likelihood of reversal “despeciation”
D
migration
“Gray zone” of speciation
Divergence
# incompatibilities
E Tipping point
Accumulation of incompatibilities,
Linea
r near tipping point, snowball effect
Nonli
Divergence
Stage 0 Stage I Stage II Stage III Stage IV
F Genome 1 Genome 1 Genome 1 Genome 1 Genome 1
Genic view of speciation

Genome 2 Genome 2 Genome 2 Genome 2 Genome 2
Divergence Genomic
Direct selection hitchhiking hitchhiking Postspeciation
G Genome-wide congealing,
FST
linkage disequilibrium
Recombination rate (r)
from selected loci
H
FST Genomic landscape of
differentiation
Mb
I Spatial perspective
fA Geographic clines
Geographic space
Figure 2. Alternative conceptual depictions of the speciation continuum. There is no implied progression from
left to right as populations can move in either direction or stage. (A) The demic perspective assigns individuals in
one of two demes, which are assumed in panels. (B) The speciation continuum depicts continuous variation in
degree of reproductive isolation (RI) with arrows indicating that this is not necessarily unidirectional (Stankowski
and Ravinet 2021). (C) The likelihood of speciation reversal may depend on the number, type, and strength of
reproductive barriers and may be narrower than the continuum of RI (Seehausen et al. 2008a; Lowry 2012). (D)
The gray zone of speciation depicts a narrow range of genetic divergence over which populations transition
rapidly between high and low likelihood of gene flow (Roux et al. 2016). (E) Hypothetical trajectories reflecting
the onset and rate of accumulation of incompatibilities during speciation, which may include both intrinsic (Orr
1995; Yamaguchi and Iwasa 2017) and extrinsic incompatibilities (Nosil et al. 2017). (F) The genic view of
speciation describes the speciation process in hypothetical stages where gene flow is initially restricted by few loci
under selection, followed by restricted gene flow of linked neutral loci until the entire genome is restricted (Wu
2001). (G) Increasing linkage disequilibrium among loci under divergent selection is a result of reduction in gene
flow, which affect more and more weakly linked loci until the entire genome has restricted gene flow (Feder et al.
2012). (H ) Levels of gene flow are visualized via the genomic landscape of divergence. The assumption is that
with low RI, elevated divergence is localized only at loci under divergent or incompatibility selection, but the
affects on neighboring neutral loci becomes apparent with higher levels of RI. The bumpy landscape shows
stochasticity due to recombination landscape, linked selection, and demography (Ravinet et al. 2017; Wolf and
Ellegren 2017). (I ) The spatial perspective is an alternative to the demic perspective. Geographic cline analyses
show the change in allele frequencies across the transition between a single continuous population to a parapatric
pair. Prior to divergent selection, loci may reflect only isolation by distance. Then, only loci under direct selection
would show steep clines (red). As more linked neutral loci (blue) are also restricted in gene flow, clines become
narrower (Endler 1977).
also follow a reversed order when homogenizing are classified as “intermediate” relative to paren-
gene flow leads to breakdown of reproductive tal species (Rieseberg et al. 1993; Thompson
barriers and ephemeral species revert to a stage et al. 2021), or as “transgressive” when they oc-
of panmixia (Fig. 1A; see references above). Al- cur outside the variation found in either paren-
though presented as such, these stages are not tal species (Slatkin and Lande 1994; Rieseberg
discrete occurrences in nature but rather used as et al. 1999b, 2003; Parsons et al. 2011; Lamich-
a model to frame the different roles evolutionary haney et al. 2018; Meier et al. 2019). Plant breed-
processes are playing at each stage. One can di- ers have long relied on hybridization and selec-
vide the speciation process in various ways but tive breeding of transgressive phenotypes to
what is important is to emphasize is what pro- obtain varieties of crops with desired extreme
cesses are being studied and why they are rele- traits. In an evolutionary context, “transgressive
vant for a particular speciation event. segregation” can give rise to new ecotypes or
species when extreme traits allow hybrid line-
ages to establish in ecological niches where pa-
ADAPTIVE AND DIVERSIFYING OUTCOMES
rental species cannot survive (Arnegard et al.
OF HYBRIDIZATION
2014; Selz and Seehausen 2019; Chhina et al.
Hybridization had long been seen as unimpor- 2022; Schluter and Rieseberg 2022). Speciation
tant in evolution or actively detrimental to bio- through transgressive segregation in ecologically
diversity through the breakdown of species relevant traits occurs in plants such as Helian-
boundaries (Mayr 1942, 1963; Coyne and Orr thus (Lexer et al. 2003; Rieseberg et al. 2003;
2004). Botanists often dissented from this view Owens et al. 2023), Senecio (Wong et al. 2022),
and recently zoologists’ perspectives have also and Arabidopsis (Clarke et al. 1995), but also in
begun to change (Mallet 2008). Although it is animals such as in the cichlid adaptive radiation
known that in some cases hybridization can (Seehausen 2004; Kagawa and Takimoto 2018).
contribute to biodiversity via reinforcement of Moreover, transgression in mating traits can
reproductive barriers (see Yukilevich et al. 2023) lead to speciation through sexual selection on
and hybrid speciation, it is unclear whether this novel traits (Kagawa et al. 2023).
is a frequent outcome. Here, we focus on how Transgression in F1 hybrids was found in
hybridization can reshuffle existing genetic var- 20% of the crosses in a meta-analysis (Thomp-
iation into novel combinations, thereby adding son et al. 2021). Transgression is most common
variation faster than that produced by de novo in polygenic traits, and can be caused by heter-
mutation, and so providing novel phenotypes osis, which masks deleterious mutations in het-
upon which selection can act (Seehausen 2004; erozygous sites, a phenomenon seen in early
Mallet 2007; Arnold et al. 2008; Hedrick 2013; generation hybrids (Rieseberg et al. 1999a;
Marques et al. 2019; Nieto Feliner et al. 2020; Kagawa and Takimoto 2018). Alternatively,
Kulmuni et al. 2023). We discuss how selection complementary gene action and “epistasis” re-
can act on novel phenotypic combinations in sulting from recombination of homozygous pa-
hybrid individuals and the potential outcomes rental alleles into novel combinations can also
of this for populations or species. We then cause transgression, an effect that persists in lat-
highlight how this may lead to bursts of pheno- er generation hybrids (Rieseberg et al. 1999a; de
typic diversity through adaptive radiation and Los Reyes 2019; Fraser 2020). Studies with later
how this diversification can persist over evolu- generation hybrids and recombinant inbred
tionary timescales. lines are useful to distinguish between these
mechanisms and assess the evolutionary signifi-
cance of transgression (Pereira et al. 2014). The
Transgressive Segregation in Phenotype and
amount of transgression is expected to increase
Gene Expression in Hybrid Individuals
either with genetic distance or (counterintui-
Hybridization can lead to novel phenotypes that tively) phenotypic similarity between parental
do not exist in parental taxa. Novel phenotypes taxa (Stelkens and Seehausen 2009; Stelkens
et al. 2009). The genetic architecture of traits can of genetic incompatibilities that counteract gene
constrain or promote transgression and trait flow (Runemark et al. 2019; Moran et al. 2021).
evolvability (Albertson and Kocher 2005; Par- For instance, introgression from Denisovans
sons et al. 2011). For instance, polygenic traits into modern humans of variant alleles enhanced
under stabilizing selection in parental popula- hypoxia resistance in Tibetan people living in
tions are likely to be transgressive in F2 progeny high altitudes (Huerta-Sánchez et al. 2014).
(Fraser 2020). In some instances, species shift into novel
Misregulation of gene expression in early environments occupied by a preadapted sister
generation hybrids is known to contribute to species, favoring adaptive introgression from
barriers to gene exchange in, for example, Dro- the resident to the newly arriving species (Sán-
sophila, sunflowers, mice, and pupfish (Landry chez-Guillén et al. 2016). For example, an in-
et al. 2007; Renaut et al. 2009; Civetta 2016; crease of invasiveness of the sunflower Helian-
Larson et al. 2017; Mack and Nachman 2017; thus annuus resulted from introgression (Yatabe
McGirr and Martin 2020; Smith et al. 2021). et al. 2007). In mammals, a rodenticide resis-
Transgressive gene expression has also been tance allele introgressed from Mus spretus into
documented in stabilized homoploid hybrid Mus musculus domesticus (Song et al. 2011). In
species of both animals and plants (Hegarty amphibians, there is evidence for adaptive intro-
et al. 2008; Papoli Yazdi et al. 2022), and novel gression from an invasive species of salamander
combinations of divergent regulatory elements into a threatened native species, following
in hybrids have resulted in novel phenotypes human-mediated introductions (Fitzpatrick
(Pavey et al. 2010; Singh and Ahi 2022). Hybrid- et al. 2010). In insects, an insecticide resistance
ization has also been suggested to deregulate allele from Anopheles coluzzi introgressed into
selfish genetic elements, such as transposable Anopheles gambiae malaria mosquitoes (Norris
elements (TEs), resulting in TE insertions dur- et al. 2015), and alleles encoding locally favored
ing meiosis, increased TE abundance, or higher mimetic color patterns introgressed between
levels of TE transcripts (Ungerer et al. 2006; multiple species of Heliconius butterflies (Heli-
Dion-Côté et al. 2014; Hénault et al. 2020; but conius Genome Consortium 2012). Adaptive
see Göbel et al. 2018). Accumulation of TEs can introgression thus appears to be fairly common
cause genome rearrangements and destabilize and facilitates adaptation and persistence of spe-
the genome (Serrato-Capuchina and Matute cies in changing environments, but more work is
2018), alter regulatory networks (Feschotte et needed to understand when hybridization and
al. 2002), or suppress the expression of genes subsequent introgression may accelerate speci-
located close to TEs (Whisson et al. 2012). The ation.
extent to which novel combinations of regulato-
ry elements and genomic rearrangements can
Hybrid Speciation, the Combinatorial View,
alter patterns of gene expression in hybrids,
and Adaptive Radiations
and how these novel phenotypes can be favored
by selection will be an exciting focus for future Hybrid speciation refers to the evolution of a
research. new species from a population formed by
hybridization between two pre-existing species.
Hybrid speciation thus leads to a net gain in
Adaptive Introgression
species, while adaptive introgression does not.
Introgression can contribute to adaptation by Hybrid speciation requires emergence of repro-
transferring favored variants between popula- ductive isolation between the population of hy-
tions. The rate of adaptive introgression is influ- brid origin and its parental species, which can
enced by presence of adaptive variation within arise as a direct consequence of admixture.
structural rearrangements (e.g., inversions), by However, because it is very difficult to convinc-
local recombination rates across the genome ingly show that it was admixture that led to re-
(Kim and Rieseberg 1999), and by the presence productive isolation to both parentals, only a few
cases of hybrid speciation are accepted by the et al. 2017a), Caribbean pupfishes (Richards
strictest definitions (Mallet 2007; Mavárez and et al. 2021), and munia birds (Stryjewski and
Linares 2008; Schumer et al. 2014b). The com- Sorenson 2017). After new or empty niches
bination of parental genetic variants may lead to are filled by this initial burst, species radiation
reproductive isolation either because they result can continue through more isolated cases of
in adaptation to a novel ecological niche where adaptive introgression or hybrid speciation gen-
parental taxa cannot survive (Rieseberg et al. erating even more phenotypic novelty that
2003), or because they result in intrinsic incom- may persist as new species (Seehausen 2004;
patibilities between the hybrid species and both Fig. 3). For instance, species within the radiation
parental species (Hermansen et al. 2014). of Darwin’s finches likely persisted through
In “allopolyploid hybrid speciation,” hy- multiple cycles of fusion and fission (Fig. 1C;
bridization is followed by chromosome dou- Grant and Grant 2008; Han et al. 2017; Rubin
bling, potentially leading to almost immediate et al. 2022). Cyclical shifts in predatory land-
reproductive isolation of hybrid species. This scape and haplotype diversity fueled by hybrid-
mode of speciation is commonly observed in ization facilitated the radiation of Daphnia in
plants (for review, see Hegarty and Hiscock northwest European lakes (Spaak and Hoekstra
2005; Soltis et al. 2014). In contrast, homoploid 1997; Gießler et al. 1999).
hybrid speciation (i.e., without chromosome
doubling) is more difficult to detect as it is
difficult to disentangle from introgression. Ad- PREDICTABILITY OF HYBRIDIZATION
vances in genomics have allowed us to sequence OUTCOMES
more species and larger portions of each ge- Despite the often-unpredictable nature of
nome, revealing new instances of homoploid evolution, some predictable patterns of hybrid-
hybrid speciation that were not apparent from ization seem to be emerging. In this section we
phenotype alone. Among the most widely ac- focus on areas of recent research. Several well-
cepted examples for homoploid hybrid specia- known patterns, like Haldane’s rule (Haldane
tion are in plants (e.g., genus Helianthus [Riese- 1922; Orr 1997) and the large X-effect (Dob-
berg et al. 1995 but see Owens et al. 2023], yeast zhansky 1937b; Coyne and Orr 2004; Payseur
[Greig et al. 2002; Leducq et al. 2016], Heliconius et al. 2018; Fraïsse and Sachdeva 2021) are
[Jiggins et al. 2008; Edelman and Mallet 2021], discussed more thoroughly in another article
Amphilophus [Olave et al. 2022, and Rhagoletis in this collection (Reifová et al. 2023). Growing
Schwarz et al. 2005]). access to genomic data has now revealed
Reassembly of old variants into new combi- new general patterns very likely driven by the
nations, “combinatorial speciation,” can give interplay between various selective pressures
rise to a radiation of diverse, ecologically differ- and recombination. These emerging predict-
entiated species, each constituting a mosaic of able evolutionary outcomes are discussed be-
parental lineages both genetically and pheno- low.
typically (Seehausen 2004; Kagawa and Taki-
moto 2018; Marques et al. 2019). These new
allelic combinations can take rapid advantage Predictability of Introgression at
of multiple empty niches resulting in a burst of the Genomic Level
phenotypic diversity that persists as discrete
species emerging from an initial hybrid swarm When divergent genomes are recombined in hy-
(Fig. 3). For example, the silversword alliance brids, multiple selective pressures are expected
was seeded by admixture giving rise to an allo- to operate in concert, which can lead to some
polyploid radiation on the Hawaiian archipela- predictable patterns of admixture. One recently
go (Barrier et al. 1999). Hybrid swarm origins discovered pattern is that recombination rate
have also been implicated in the rapid radiations tends to be positively correlated with the fraction
of Lake Victoria region cichlid fishes (Meier of introgressed alleles in a genomic region
Upper Nile lineage Congolese lineage
Initiation of
adaptive radiation
through hybrid swarm
B Progression of
adaptive radiation
P. pundamilia P. nyererei
(western Mwanza Gulf) (Makobe Island)
P. sp. “pundamilia-like” P. sp. “nyererei-like”

Adaptive introgression Hybrid speciation
Figure 3. Hybridization can facilitate adaptive radiation. Admixture variation from distantly related species can
fuel (A) the onset of adaptive radiation, whereby a genetically diverse hybrid swarm gives rise to ecologically
diverse species that constitute different genomic mosaics of the parental lineages. The downward pyramids of
arrows depict multiple generations of hybridization; and (B) the continuation of adaptive radiation, whereby loci
affecting ecological adaptation and assortative mating are exchanged and recombined to form novel trait com-
binations. This can occur through adaptive introgression where a novel trait emerges in one species due to gene
flow from another or through hybrid speciation (Meier et al. 2017b) where admixed lineages with new combi-
nations of parental alleles evolve into separate species.
(Nachman and Payseur 2012; Schumer et al. Recent theory suggests that another important
2018; Leitwein et al. 2019; Martin et al. 2019; factor is the reduction of ancestry variance due
Dreissig et al. 2020; Calfee et al. 2021; Duranton to recombination in later hybrid generations.
and Pool 2022). This correlation is believed to be Due to large variance in fitness, deleterious mul-
caused partly by linked selection: if incompati- tilocus variation is removed more effectively in
bilities are multilocus and scattered evenly large blocks soon after introgression, rather than
around the genome, selection against incompat- later, when recombination already has reduced
ible alleles tends to purge larger blocks of linked ancestry variance and therefore reduced vari-
neutral alleles where recombination rate is low. ance in fitness (Veller et al. 2023). An interesting
corollary prediction is that species with many species boundaries. For example, many known
chromosomes, such as humans, and therefore cases of adaptive introgression involve herbicide
high genome-wide average recombination rates, or pesticide resistance where the introgressed
will purge deleterious introgressed variation less alleles have major effects on survival (Whitney
quickly than species with few chromosomes, like et al. 2006; Heliconius Genome Consortium
Drosophila (Veller et al. 2023). However, an op- 2012; Clarkson et al. 2014; Valencia-Montoya
posite pattern has sometimes been shown where et al. 2020). In humans, genomic regions asso-
there is more introgression in low recombin- ciated with gene expression are purged from ar-
ing regions (Duranton and Pool 2022), a sig- chaic introgression, suggesting that altered gene
nal that could arise if selection favors intro- regulation had deleterious effects on the pheno-
gression. Expectations about the correlation be- type (Telis et al. 2020; Vilgalys et al. 2022).
tween recombination rate and introgression are The purging is most pronounced for highly
still mixed, and more work is needed to clarify pleiotropic enhancers (Telis et al. 2020). In hy-
the topic. bridizing ants, haplotypes with signatures of
A second pattern that is beginning to emerge past positive selection are more likely to fix in
is that, when one of the hybridizing species has a hybrids (Nouhaud et al. 2022) and due to vari-
smaller effective population size Ne, that species ous selective pressures acting in concert genome
is more likely to fix slightly deleterious alleles evolution after hybridization is repeatable across
due to genetic drift. As a result, the species natural population replicates (Fig. 4). In early
with the smaller Ne tends to be a recipient of generation hybrids, introgressed loci will be em-
introgression, rather than a donor. Upon hy- bedded within large haplotype blocks and the
bridization, deleterious alleles can be purged rate of introgression of these blocks will depend
by introgression of beneficial alleles from the on the balance between beneficial and deleteri-
species with larger Ne (Harris and Nielsen ous alleles within the block (Sachdeva and
2016; Schumer et al. 2018; Nouhaud et al. 2022). Barton 2018).
In a third pattern, when incompatibilities
are strong, they will be purged and homospecific
Predictability of Hybridization Outcomes at
allele combinations fixed at the incompatible
the Level of Fitness
loci. For example, introgression tends to be
rare at nuclear-encoded mitochondrial-local- Long-term outcomes of hybridization depend
ized genes. Due to the uniparental inheritance on overall fitness of hybrids. Early generations
of mitochondria, heterospecific combinations of of hybridization tend to show the strongest hy-
nuclear-encoded mitochondrial proteins and brid breakdown (Bank et al. 2012). Dominant
mitochondrial-encoded proteins can become incompatibilities will appear in the F1 genera-
incompatible (Barr and Fishman 2010; Trier tion, while recessive incompatibilities will be-
et al. 2014; Chang et al. 2015; Gaborieau et al. come exposed to natural selection in later hybrid
2016; McFarlane et al. 2016; Shipley et al. 2016; generations (Reifová et al. 2023). If incompati-
Pereira et al. 2021). Heterospecific combinations bilities are strong and do not have an ecological
of these proteins may lead to suboptimal respi- component they are expected to be purged early
ration (McFarlane et al. 2016; Shipley et al. 2016; (Bank et al. 2012). Incompatibilities are purged
Wagner et al. 2020). Thus, selection tends to from Tigriopus copepod recombinant inbred
favor homospecific combinations, purging the lines in a few generations of recombination,
mismatched allele even if it comes from the spe- which then recover fitness on par with parents
cies contributing the majority of genomic DNA (Pereira et al. 2014). However, in some cases,
(Runemark et al. 2018). incompatibilities are environment-dependent
Allelic effect size, pleiotropy, and past selec- so that hybrids experience a reduced fitness in
tive regimes can also affect the likelihood of in- one environment but not in another (Arnegard
trogression. If hybrid fitness is low, only alleles et al. 2014; Kulmuni et al. 2020; Thompson et al.
under very strong positive selection can cross 2022). For example, in yeast, 24% of viable cross-
A Topologies Hybrid
F. aquilonia
Hybrid
F. polyctena
F. aquilonia
F. polyctena
B
F. polyctena F. aquillonia Hybrid
Outgroup Outgroup Outgroup P. hispaniolensis
P. domesticus P. italiae
100
Admixture proportions (K = 2)
1
LånR
Crete
Topology weighting
0 0
100 1
Corsica
LånW
0 0
100 1
Sicily
Pik
0 0
100 1
Malta
Bun
0 0
Chr13 ChrZ
Figure 4. Examples of predictable genomic patterns after hybridization. Dark gray squares highlight specific
regions where repeatability is qualitatively observed. (A) Hybridization between wood ants Formica aquilonia
and Formica polyctena has led to correlated patterns of ancestry from the parental species across the genome in
four independent hybrid lineages: LånR, LånW, Pik, and Bun. As an example, we show the first half of Chro-
mosome 13, but similar correlated patterns of ancestry are found across the genome (Nouhaud et al. 2022). (B)
Repeated instances of hybridization between the house sparrow (Passer domesticus; to the left in the row) and the
Spanish sparrow (Passer hispaniolensis; middle) led to the generation of hybrid lineages (called the Italian
sparrow, Passer italiae; right) on four Mediterranean islands. Here, ancestry is illustrated as a sliding window
admixture assignment. While the lineages differ in overall contribution from each parent species, some genomic
regions are inherited from the house sparrow in all four lineages as seen above. In these regions, there is an
enrichment of mitonuclear genes and DNA-repair genes (Runemark et al. 2018).
es become deleterious when tested in another or counteract speciation deserves attention from
environment (Hou et al. 2015). Hybrid fitness future studies.
has often been measured in the environment of
the parental species, where hybrids may suffer
CONCLUDING REMARKS
from inviability or sterility relative to parental
species (Coyne and Orr 2004). However, in a Many new insights into outcomes and evolu-
novel environment, hybrids may even enjoy a tionary consequences of hybridization have
fitness advantage compared with parental spe- been gained in the genomics era. We now
cies in spite of intrinsic incompatibilities (Kul- know that hybridization is widespread among
muni et al. 2023). The extent of hybrid unfitness plants and animals alike, that it can be an im-
and hybrid breakdown is broadly correlated portant source of genetic and phenotypic varia-
with the degree of genetic differentiation. Yet, tion, and that it can be a target of selection,
yeast can produce viable F1 hybrids even be- facilitating species formation and persistence.
tween species with 10%–20% nucleotide diver- Historical hybridization events have fueled
gence (Brice et al. 2021) and even though many some of the fastest bursts of diversification in
F2 hybrids are inviable, some persist (Stelkens animals (Meier et al. 2017a), and ongoing intro-
and Bendixsen 2022). “Hybrid vigor” (hetero- gression continues to provide variants that are
sis), in contrast, is expected between less differ- favored by sexual and environmental selection
entiated lineages and is dependent on the extent (Fitzpatrick et al. 2010; Heliconius Genome
to which hybridization breaks down beneficial Consortium 2012), facilitating species persis-
or deleterious parental allele combinations tence in an ever-changing environment. As we
(Dagilis et al. 2019). Heterosis across many hy- discover more about the role of hybridization in
brid classes (F1, F2, etc.) is predicted to occur speciation some old questions remain, while
when parental lineages are highly inbred (Simon new questions begin to arise (Box 2).
et al. 2018). The extent to which hybrid break- These questions and continued technologi-
down interacts with hybrid heterosis to facilitate cal progress in genomics prompt the need for
complementary advances in theory and meth- 2016; Meier et al. 2021). Finally, tackling the
ods. We need analytical tools to improve identi- long-standing challenge to differentiate between
fication of conditions under which hybridization shared alleles due to incomplete lineage sorting
can lead to novelty and in which environments or hybridization between sister taxa will allow for
this might be advantageous, neutral, or disad- a more transferrable metric of gene flow across
vantageous. It would also be beneficial to be different levels of divergence.
able to analyze hybridization and gene flow while The role of hybridization in speciation is
taking into account two-dimensional space, ge- multifaceted. As we investigate the evolutionary
netic architecture of traits, and recent demogra- processes shaping the Tree of Life, we reveal
phy. Recent improvements in long-range se- more complexity in the role that hybridization
quencing would benefit from complementary plays during and after speciation. More studies
software that incorporates haplotype block anal- across systems will reveal broad patterns we may
yses in hybridization studies (Sedghifar et al. expect under certain sets of conditions. As we
BOX 2. OPEN QUESTIONS FOR FUTURE RESEARCH
• How does the likelihood of hybridization vary across higher levels of taxonomic organization (e.g.,
species, genus, family) and taxonomic groups (e.g., animals, plants, fungi, protists)?
• How do different life history traits (e.g., sex determination, mating systems) affect the likelihood of
hybridization?
• Does shared extrinsic environment (e.g., climatic history) affect hybridization across codistributed
population or species pairs in suture zones similarly, despite different intrinsic factors (e.g., dis-
persal rates)?
• How does demographic history (e.g., range expansions or contractions) interact with selection (e.g.,
purging of deleterious mutations) during hybridization?
• Do incompatibilities caused by different selective regimes (e.g., intragenomic incompatibilities,
ecological incompatibilities, mate preference incompatibilities) evolve in different ways or can they
be generalized under the BDMI model? And how can they facilitate the evolution of each other and
restrict gene flow between incipient species?
• How do our predictions change if we expand from a simple two-deme model to a more realistic
model of speciation where a species is a set of multiple potentially hybridizing populations dis-
tributed across space?
• How general is the pattern of a “tipping point” in speciation and what factors (e.g., neutral and
adaptive) influence its occurrence?
• How does allelic reshuffling by hybridization alter gene regulation to give rise to novel phenotypes
and barriers to gene flow?
• To what extent can genomic rearrangements change gene expression in hybrids and how adaptive
is this phenotypic variation?
• When does hybridization and introgression aid in species persistence versus speciation?
• What is the interplay between recombination, introgression, and selection, and how does this
impact evolutionary consequences of hybridization?
• How does the genomic architecture of adaptive phenotypes promote or constrain the evolution of
novelty and new species via hybridization?
• To what extent does the interplay between hybrid breakdown and heterosis influence speciation
and species persistence?
revisit classic theory with modern methods and tion. Cold Spring Harb Perspect Biol doi:10.1101/
cshperspect.a041435
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The Role of Hybridization in Species Formation and Persistence

Joshua V. Peñalba, Anna Runemark, Joana I. Meier, Pooja Singh, Guinevere O.U. Wogan, Rosa
Sánchez-Guillén, James Mallet, Sina J. Rometsch, Mitra Menon, Ole Seehausen, Jonna Kulmuni and
Ricardo J. Pereira
Cold Spring Harb Perspect Biol published online March 4, 2024
Subject Collection Speciation
The Role of Hybridization in Species Formation Structural Variants and Speciation: Multiple
and Persistence Processes at Play
Joshua V. Peñalba, Anna Runemark, Joana I. Emma L. Berdan, Thomas G. Aubier, Salvatore
Meier, et al. Cozzolino, et al.
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For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/
Quantitative Analyses of Coupling in Hybrid The Impact of Chromosomal Rearrangements in

Zones Speciation: From Micro- to Macroevolution
Thomas J. Firneno, Jr., Georgy Semenov, Erik B. Kay Lucek, Mabel D. Giménez, Mathieu Joron, et
Dopman, et al. al.
For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

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The Role of Hybridization in Species Formation

Joshua V. Peñalba,1 Anna Runemark,2 Joana I. Meier,3,4 Pooja Singh,5,6

Hybridization, or interbreeding between different taxa, was traditionally considered to be rare

J.V. Peñalba et al.

T he origin of species and the role that “hybrid-

Role of Hybridization in Species Formation

J.V. Peñalba et al.

A Species formation in time B Species as metapopulations

C Phenotypic change over time D Phenotypic change over space

Role of Hybridization in Species Formation

J.V. Peñalba et al.

fects) of these incompatibilities will determine INSIGHTS ABOUT SPECIES BOUNDARIES

Role of Hybridization in Species Formation

Population 1 Species 1 Demic perspective

“Gray zone” of speciation

Genic view of speciation

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Upper Nile lineage Congolese lineage

P. sp. “pundamilia-like” P. sp. “nyererei-like”

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Role of Hybridization in Species Formation

BOX 2. OPEN QUESTIONS FOR FUTURE RESEARCH

J.V. Peñalba et al.

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Role of Hybridization in Species Formation

J.V. Peñalba et al.

Role of Hybridization in Species Formation

J.V. Peñalba et al.

The Role of Hybridization in Species Formation and Persistence

Cold Spring Harb Perspect Biol published online March 4, 2024

Subject Collection Speciation

For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

Quantitative Analyses of Coupling in Hybrid The Impact of Chromosomal Rearrangements in

For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

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